Cited by 1,136Autophagy in Disease and TherapyMetabolism, Diabetes, and CancerMuscle Physiology and Disorders

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Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis

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He, Congcong, Bassik, Michael C., Moresi, Viviana, Sun, Kai, Wei, Yongjie, Zou, Zhongju, An, Zhenyi, Loh, Joy, Fisher, Jill, Sun, Qihua, Korsmeyer, Stanley, Packer, Milton, May, Herman I., Hill, Joseph A., Virgin, Herbert W., Gilpin, Christopher, Xiao, Guanghua, Bassel-Duby, Rhonda, Scherer, Philipp E., Levine, Beth·2012·Nature

DOI 10.1038/nature10758PMC PMC3518436

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Abstract

Exercise has beneficial effects on human health, including protection against metabolic disorders such as diabetes. However, the cellular mechanisms underlying these effects are incompletely understood. The lysosomal degradation pathway, autophagy, is an intracellular recycling system that functions during basal conditions in organelle and protein quality control. During stress, increased levels of autophagy permit cells to adapt to changing nutritional and energy demands through protein catabolism. Moreover, in animal models, autophagy protects against diseases such as cancer, neurodegenerative disorders, infections, inflammatory diseases, ageing and insulin resistance. Here we show that acute exercise induces autophagy in skeletal and cardiac muscle of fed mice. To investigate the role of exercise-mediated autophagy in vivo, we generated mutant mice that show normal levels of basal autophagy but are deficient in stimulus (exercise- or starvation)-induced autophagy. These mice (termed BCL2 AAA mice) contain knock-in mutations in BCL2 phosphorylation sites (Thr69Ala, Ser70Ala and Ser84Ala) that prevent stimulus-induced disruption of the BCL2-beclin-1 complex and autophagy activation. BCL2 AAA mice show decreased endurance and altered glucose metabolism during acute exercise, as well as impaired chronic exercise-mediated protection against high-fat-diet-induced glucose intolerance. Thus, exercise induces autophagy, BCL2 is a crucial regulator of exercise- (and starvation)-induced autophagy in vivo, and autophagy induction may contribute to the beneficial metabolic effects of exercise.

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Positional cloning of the mouse obese gene and its human homologue
Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., & Friedman, J. M. (1994) · Nature · doi:10.1038/372425a0 · Cited by 13,419
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Levine, B., & Kroemer, G. (2008) · Cell · doi:10.1016/j.cell.2007.12.018 · Cited by 7,069
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Dong, X., & Levine, B. (2013) · Journal of Innate Immunity · doi:10.1159/000346388 · Cited by 4,444
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Moy, R. H., & Cherry, S. R. (2013) · Journal of Innate Immunity · doi:10.1159/000350326 · Cited by 3,551
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Scherer, P. E., Williams, S. P., Fogliano, M., Baldini, G., & Lodish, H. F. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.45.26746 · Cited by 3,238
Self-citation
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Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E.-L., Mizushima, N., Ohsumi, Y., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20039 · Cited by 2,311
Self-citation
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Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., & Ohsumi, Y. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-09-0704 · Cited by 2,105
Leptin levels reflect body lipid content in mice: Evidence for diet-induced resistance to leptin action
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Leite, J. S. M., Cruzat, V. F., Krause, M. D. S., & de Bittencourt, P. I. H. (2016) · Nutrire · doi:10.1186/s41110-016-0021-y · Cited by 41
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Yang, S., Wang, M., Yang, L., Li, Y., Ma, Y., Peng, X., Li, X., Li, B., Jin, H., & Li, H. (2020) · OncoTargets and Therapy · doi:10.2147/ott.s247655 · Cited by 40
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Wang, B., Liu, J., Wang, Q., Arhatte, M., Cheong, L. Y., Glogowska, E., Jiang, X., Chung, S. K., Jin, L., Hu, Q., et al. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02455-w · Cited by 40
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Liu, Y., Xu, F., Liu, S., Liu, G., Yang, X., Gao, W., Fan, K., Zhao, H., & Ma, J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109971 · Cited by 40
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Yang, B. L., Yang, N., Chen, Y., Zhu, M., Lian, Y., Xiong, Z., Wang, B., Feng, L., & Jia, X. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.580978 · Cited by 39
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Yadav, R. K., Lee, G., Lee, H.-Y., Li, B., Jung, H.-E., Rashid, H.-O., Choi, M. K., Yadav, B. K., Kim, W. H., Kim, K., et al. (2015) · Autophagy · doi:10.1080/15548627.2015.1082021 · Cited by 38
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Henriksen, T. I., Wigge, L., Nielsen, J., Pedersen, B. K., Sandri, M., & Schéele, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-44535-2 · Cited by 33
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Ageing in relation to skeletal muscle dysfunction: redox homoeostasis to regulation of gene expression
Goljanek‐Whysall, K., Iwanejko, L., Vasilaki, A., Pekovic‐Vaughan, V., & McDonagh, B. (2016) · Mammalian Genome · doi:10.1007/s00335-016-9643-x · Cited by 34
Macroautophagy inhibition maintains fragmented mitochondria to foster T cell receptor‐dependent apoptosis
Corrado, M., Mariotti, F. R., Trapani, L., Taraborrelli, L., Nazio, F., Cianfanelli, V., Soriano, M. E., Schrepfer, E., Cecconi, F., Scorrano, L., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201593727 · Cited by 31
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Komine, S., Akiyama, K., Warabi, E., Oh, S., Kuga, K., Ishige, K., Togashi, S., Yanagawa, T., & Shoda, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-12358-8 · Cited by 31
Multiple recycling routes: Canonical vs. non-canonical mitophagy in the heart
Moyzis, A. G., & Gustafsson, Å. B. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.09.034 · Cited by 33
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Loos, B., Klionsky, D. J., du Toit, A., & Hofmeyr, J. S. (2019) · Autophagy · doi:10.1080/15548627.2019.1687211 · Cited by 32
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Tiong, H. T., Fan, D., Frampton, C., Ananthakrishnan, A. N., & Gearry, R. B. (2024) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjae053 · Cited by 30
HDAC2 promotes autophagy-associated HCC malignant progression by transcriptionally activating LAPTM4B
Wang, M., Liao, J., Wang, J., Xu, M., Cheng, Y., Wei, L., & Huang, A. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06981-3 · Cited by 30
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Chang, H., Peng, X., Xia, Y., Zhang, J., Xu, S., Wang, H., Wang, Z., Ma, X., & Gao, Y. (2019) · Journal of Comparative Physiology B · doi:10.1007/s00360-019-01245-5 · Cited by 31
Impact of Different Physical Exercises on the Expression of Autophagy Markers in Mice
Pinto, A. P., da Rocha, A. L., Marafon, B. B., Rovina, R. L., Muñoz, V. R., da Silva, L. E. C. M., Pauli, J. R., de Moura, L. P., Cintra, D. E., Ropelle, E. R., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052635 · Cited by 30
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Gordon, J. W., Dolinsky, V. W., Mughal, W., Gordon, G. R., & McGavock, J. (2015) · Biochemistry and Cell Biology · doi:10.1139/bcb-2015-0012 · Cited by 30
Role of gp130 in basal and exercise-trained skeletal muscle mitochondrial quality control
Fix, D. K., Hardee, J. P., Gao, S., VanderVeen, B. N., Velázquez, K. T., & Carson, J. A. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01063.2017 · Cited by 31
Mitophagy modulation for the treatment of cardiovascular diseases
Forte, M., D’Ambrosio, L., Schiattarella, G. G., Salerno, N., Perrone, M. A., Loffredo, F. S., Bertero, E., Pilichou, K., Manno, G., Valenti, V., et al. (2024) · European Journal of Clinical Investigation · doi:10.1111/eci.14199 · Cited by 29
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He, A., Pu, Y., Jia, C., Wu, M., He, H., & Xia, Y. (2024) · Sports Medicine · doi:10.1007/s40279-024-02031-2 · Cited by 31
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Differential Response of Hippocampal and Cerebrocortical Autophagy and Ketone Body Metabolism to the Ketogenic Diet
Liśkiewicz, D., Liśkiewicz, A., Nowacka-Chmielewska, M. M., Grabowski, M., Pondel, N., Grabowska, K., Student, S., Barski, J. J., & Małecki, A. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.733607 · Cited by 29
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Maiese, K. (2023) · Current Neurovascular Research · doi:10.2174/1567202620666230721122957 · Cited by 30
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Kuno, A., & Horio, Y. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/6714686 · Cited by 29
Proteomic strategies to unravel age-related redox signalling defects in skeletal muscle
Cobley, J. N., Sakellariou, G. K., Husi, H., & McDonagh, B. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.09.012 · Cited by 32
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Sun, M., Tan, Y., Rexiati, M., Dong, M., & Guo, W. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.09.004 · Cited by 31
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Min, S. Y., Learnard, H., Kant, S., Gealikman, O., Rojas-Rodriguez, R., DeSouza, T., Desai, A., Keaney, J. F., Corvera, S., & Craige, S. M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20082046 · Cited by 29
Exercise Improves the Coordination of the Mitochondrial Unfolded Protein Response and Mitophagy in Aging Skeletal Muscle
Wang, Y., Li, J., Zhang, Z., Wang, R., Hai, B., & Zhang, Y. (2023) · Life · doi:10.3390/life13041006 · Cited by 29

Authors: He, C., Bassik, M. C., Moresi, V., Sun, K., Wei, Y., Zou, Z., An, Z., Loh, J., Fisher, J., Sun, Q., Korsmeyer, S., Packer, M., May, H. I., Hill, J. A., Virgin, H. W., Gilpin, C., Xiao, G., Bassel-Duby, R., Scherer, P. E., & Levine, B.
Affiliations: The University of Texas Southwestern Medical Center (US)
Dana-Farber Cancer Institute (US)
Howard Hughes Medical Institute (US)
Washington University in St. Louis (US)
Corresponding author: Levine, Beth
ORCID: He, Congcong
Bassik, Michael C.
Moresi, Viviana
Sun, Kai
Zou, Zhongju
Packer, Milton
May, Herman I.
Hill, Joseph A.
Virgin, Herbert W.
Gilpin, Christopher
Xiao, Guanghua
Scherer, Philipp E.
Levine, Beth
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-01-18
Volume: 481
Issue: 7382
Pages: 511-515
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature10758
PMC: PMC3518436
OpenAlex: W2082476985
Cited by: 1,136
References: 36
Citations by year: 2026: 40 · 2025: 47 · 2024: 49 · 2023: 55 · 2022: 64 · 2021: 90 · 2020: 93 · 2019: 76 · 2018: 93 · 2017: 99 · 2016: 94 · 2015: 112 · 2014: 82 · 2013: 80 · 2012: 61
FWCI: 79.93
Type: journal article
Language: en
Update notices: erratum (2013-11-06)
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
Funders: Howard Hughes Medical Institute
National Heart, Lung, and Blood Institute (R0I HL090842, R0I HL080244, R01HL090842)
National Cancer Institute (R01CA112023, R01CA109618, P30CA142543)
National Institute of Allergy and Infectious Diseases (R01AI084887, R0I AI084887)
National Institute of Diabetes and Digestive and Kidney Diseases (RCI DK086629, R01DK055758, 1P01 DK0887761, RC1DK086629, P01DK088761)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: Bcl-2, Bcl-2 phosphorylation, skeletal muscle, myocardium, glucose metabolism, impaired glucose tolerance, high-fat diet, endurance, starvation-induced autophagy, exercise metabolism, diabetes protection
MeSH terms: Beclin-1, Animals, Autophagy, Cells, Cultured, Dietary Fats, Physical Exertion, Food Deprivation, Glucose, Glucose Tolerance Test, Homeostasis, Male, Mice, Transgenic, Mutation, Myocardium, Phosphorylation, Physical Conditioning, Animal, Physical Endurance, Protein Binding, Proto-Oncogene Proteins, Running, Glucose Intolerance, Muscle, Skeletal, Proto-Oncogene Proteins c-bcl-2, Leptin, Apoptosis Regulatory Proteins, Mice, Adiponectin, Gene Knock-In Techniques

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Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis

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